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Cis and trans regulatory divergence underlies phenotypic and evolutionary diversification. Relatively little is understood about the complexity of regulatory evolution accompanying crop domestication, particularly for polyploid plants. Here, we compare the fiber transcriptomes between wild and domesticated cotton ( Gossypium hirsutum ) and their reciprocal F 1 hybrids, revealing genome-wide (~15%) and often compensatory cis and trans regulatory changes under divergence and domestication. The high level of trans evolution (54%–64%) observed is likely enabled by genomic redundancy following polyploidy. Our results reveal that regulatory variation is significantly associated with sequence evolution, inheritance of parental expression patterns, co-expression gene network properties, and genomic loci responsible for domestication traits. With respect to regulatory evolution, the two subgenomes of allotetraploid cotton are often uncoupled. Overall, our work underscores the complexity of regulatory evolution during fiber domestication and may facilitate new approaches for improving cotton and other polyploid plants. Relatively little is known about the complexity of regulatory evolution accompanying polyploid crop domestication. Here, using reciprocal hybrids between wild and domesticated allotetraploid cotton lines, the authors catalog cis and trans regulatory variants and show their equivalent effects on cotton fiber domestication.

Cotton fiber provides the predominant plant textile in the world, and it is also a model for plant cell wall biosynthesis. The development of the single-celled cotton fiber takes place across several overlapping but discrete stages, including fiber initiation, elongation, the transition from elongation to secondary cell wall formation, cell wall thickening, and maturation and cell death. During each stage, the developing fiber undergoes a complex restructuring of genome-wide gene expression change and physiological/biosynthetic processes, which ultimately generate a strikingly elongated and nearly pure cellulose product that forms the basis of the global cotton industry. Here, we provide an overview of this developmental process focusing both on its temporal as well as evolutionary dimensions. We suggest potential avenues for further improvement of cotton as a crop plant.

Phenotypic diversity and evolutionary innovation ultimately trace to variation in genomic sequence and rewiring of regulatory networks. Here, we constructed a pan-genome of the Gossypium genus using ten representative diploid genomes. We document the genomic evolutionary history and the impact of lineage-specific transposon amplification on differential genome composition. The pan-3D genome reveals evolutionary connections between transposon-driven genome size variation and both higher-order chromatin structure reorganization and the rewiring of chromatin interactome. We linked changes in chromatin structures to phenotypic differences in cotton fiber and identified regulatory variations that decode the genetic basis of fiber length, the latter enabled by sequencing 1,005 transcriptomes during fiber development. We showcase how pan-genomic, pan-3D genomic and genetic regulatory data serve as a resource for delineating the evolutionary basis of spinnable cotton fiber. Our work provides insights into the evolution of genome organization and regulation and will inform cotton improvement by enabling regulome-based approaches. Pan-genome and pan-3D genome analyses of the Gossypium genus reveal evolutionary relationships among transposon-driven genome expansion and chromatin topology innovation and regulatory variations for cotton fiber development.

Allotetraploid cotton (Gossypium) species represents a model system for the study of plant polyploidy, molecular evolution, and domestication. Here, chromosome-scale genome sequences were obtained and assembled for two recently described wild species of tetraploid cotton, Gossypium ekmanianum [(AD)6, Ge] and Gossypium stephensii [(AD)7, Gs], and one early form of domesticated Gossypium hirsutum, race punctatum [(AD)1, Ghp]. Based on phylogenomic analysis, we provide a dated whole-genome level perspective for the evolution of the tetraploid Gossypium clade and resolved the evolutionary relationships of Gs, Ge, and domesticated G. hirsutum. We describe genomic structural variation that arose during Gossypium evolution and describe its correlates— including phenotypic differentiation, genetic isolation, and genetic convergence— that contributed to cotton biodiversity and cotton domestication. Presence/absence variation is prominent in causing cotton genomic structural variations. A presence/ absence variation-derived gene encoding a phosphopeptide-binding protein is implicated in increasing fiber length during cotton domestication. The relatively unimproved Ghp offers the potential for gene discovery related to adaptation to environmental challenges. Expanded gene families enoyl-CoA δ isomerase 3 and RAP2-7 may have contributed to abiotic stress tolerance, possibly by targeting plant hormone-associated biochemical pathways. Our results generate a genomic context for a better understanding of cotton evolution and for agriculture.

Cotton is an agriculturally important crop. Because of its importance, a genome sequence of a diploid cotton species (Gossypium raimondii, D-genome) was first assembled using Sanger sequencing data in 2012. Improvements to DNA sequencing technology have improved accuracy and correctness of assembled genome sequences. Here we report a new de novo genome assembly of G. raimondii and its close relative G. turneri. The two genomes were assembled to a chromosome level using PacBio long-read technology, HiC, and Bionano optical mapping. This report corrects some minor assembly errors found in the Sanger assembly of G. raimondii. We also compare the genome sequences of these two species for gene composition, repetitive element composition, and collinearity. Most of the identified structural rearrangements between these two species are due to intra-chromosomal inversions. More inversions were found in the G. turneri genome sequence than the G. raimondii genome sequence. These findings and updates to the D-genome sequence will improve accuracy and translation of genomics to cotton breeding and genetics.

Background Transposable elements are major components of plant genomes and major drivers of plant genome evolution. The cotton genus ( Gossypium ) is an excellent evolutionary model for polyploidization, speciation, domestication, and crop improvement. Here, we implement genome and pangenome analyses to study in detail the dynamics of LTR-retrotransposons during the cotton evolution. Results We show that some LTR-retrotransposon lineages amplified in tetraploid cotton compared to their diploid progenitors, whereas others stayed stable or amplified but were removed through solo-LTR formation . Using species-level pangenomes we show that only a few lineages (CRM, Tekay, Ivana, and Tork) remained active after polyploidization and are still transposing. Tekay and CRM elements have re-shaped the centromeric and pericentromeric regions of tetraploid cottons in a subgenome specific manner, through new insertions but also selective eliminations through solo-LTR formation. On the other hand, Ivana and Tork have actively inserted within or close to genes affecting their expression. Finally, population-level analyses using the two pangenomes and data from 283 and 223 varieties of G. hirsutum and G. barbadense reveal changes in Transposon Insertion Polymorphism frequencies accompanying domestication and improvement of both species, suggesting the possibility of selection on linked regions. Conclusions Our findings reveal that LTR-retrotransposon lineages followed differential dynamics during cotton evolution, displaying differences among species and the two coresident genomes of allopolyploid cotton. A handful of the LTR-retrotransposon lineages that expanded after polyploidization helped shape the genomes of both G. hirsutum and G. barbadense , impacting their centromere and pericentromeric regions as well as protein-coding genes.

Gossypium barbadense is renowned for its superior fiber quality, particularly its extra-long fibers, although its fiber yield is lower compared to G. hirsutum . Here, to further reveal fiber-related genomic variants of G. barbadense , we de novo assemble 12 genomes of G. barbadense that span the wild-to-domesticated continuum, and construct a graph-based pangenome by integrating these assemblies and 17 publicly available tetraploid cotton genome assemblies. We uncover the divergent evolutionary trajectories and subsequent exchanges between G. barbadense and G. hirsutum through investigation of structural variants (SVs). We perform the SV-based GWAS analysis in G. barbadense and identify four, three, and seven candidate SVs for fiber length, fiber strength, and lint percentage, respectively. Furthermore, we detect the underlying candidate genes and uncover the origin and distribution of favorable alleles, and reveal the tradeoff between lint percentage and fiber quality. These pangenome and trait-associated SVs provide insights into and resources for improving cotton fiber. Comparing to Gossypium hirsutum , G. barbadense cotton lines have superior fiber quality but lower fiber yield. Here, the authors construct pangenome using 12 newly assembled G. barbadense genomes and 17 publicly tetraploid cotton genomes and reveal yield- and fiber-related diversity and interspecific gene flow.

The two cultivated allopolyploid cottons, Gossypium hirsutum and Gossypium barbadense, represent a remarkable example of parallel independent domestication, both involving dramatic morphological transformations under selection from wild perennial plants to annualized row crops. Deep resequencing of 643 newly sampled accessions spanning the wild‐to‐domesticated continuum of both species, and their allopolyploid relatives, are combined with existing data to resolve species relationships and elucidate multiple aspects of their parallel domestication. It is confirmed that wild G. hirsutum and G. barbadense were initially domesticated in the Yucatan Peninsula and NW South America, respectively, and subsequently spread under domestication over 4000–8000 years to encompass most of the American tropics. A robust phylogenomic analysis of infraspecific relationships in each species is presented, quantify genetic diversity in both, and describe genetic bottlenecks associated with domestication and subsequent diffusion. As these species became sympatric over the last several millennia, pervasive genome‐wide bidirectional introgression occurred, often with striking asymmetries involving the two co‐resident genomes of these allopolyploids. Diversity scans revealed genomic regions and genes unknowingly targeted during domestication and additional subgenomic asymmetries. These analyses provide a comprehensive depiction of the origin, divergence, and adaptation of cotton, and serve as a rich resource for cotton improvement. To elucidate the history of parallel domestication in Gossypium hirsutum and Gossypium barbadense, a diverse assemblage of plants spanning the wild‐to‐domesticated continuum is resequenced. A robust phylogenomic analysis of infraspecific relationships is presented, quantify patterns of genetic diversity in different gene pools, describe genetic bottlenecks associated with domestication and diffusion, detect pervasive genome‐wide bidirectional introgression and signatures of domestication.

Background Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum : A 2 and G. raimondii : D 5 ). Results Extensive IGT events exist for both diploid and allotetraploid cotton ( Gossypium ) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6 - trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. Conclusions This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution.

Two other papers focused on the plant gene expression process and functional gene mining by using transcriptomics, metabolomics, and resequencing data with the genome-wide association method. According to their specific research directions, these six articles are summarized. [...]Nie et al.reviewed research progresses and molecular mechanisms of male sterility regulated by non-coding RNAs (ncRNAs) from the perspective of high-throughput sequencing technology.